Paper in:

Patrick N. Wyse Jackson & Mary E. Spencer Jones (eds) (2002) Annals of Bryozoology: aspects of the history of research on bryozoans. International Bryozoology Association, Dublin, pp. viii+381. COLONIAL BEHAVIOUR IN 185 Colonial behaviour and group zooidal reactions in Bryozoa: history of research

Andrew N. Ostrovsky* and Natalia N. Shunatova Department of Invertebrate Zoology, Faculty of Biology and Soil Science, St. Petersburg State University, Universitetskaja nab. 7/9, St. Petersburg, 199034, Russia *Present address: Institut für Geowissenschaften, Christian-Albrechts-Universität zu Kiel, Olshausenstr. 40, 24118 Kiel, Germany

1. Introduction 2. Early studies 3. Twentieth century studies 4. Conclusions 5. Acknowledgements

1. Introduction

Investigations of modular systems encompass many colonial organisms with a high level of morphological and physiological integration. Bryozoan colonies are a very promising model in this respect, and studies of colonial behaviour are one of the approaches in evaluating the degree of colonial integration. Bryozoans demonstrate a variety of group behavioural reactions which are connected with different vital functions. Co-ordinated activities of polypides are regulated neurophysiologically, physiologically, structurally and, possibly, hormonally. Different manifestations of the regulatory mechanisms have been studied previously, and we here present a review that discusses the history of these investigations.

2. Early studies

Henry Baker was probably the first who noted in passing colonial behavioural reactions in fresh-water bryozoans (possibly, Plumatella).1 Barthelemy Dumortier described retraction of all polypides in a colony of the phylactolaemate Lophopus crystallinus (Pallas) after a stimulus was applied to a ‘coenoecium’.2 Contact with a single lophophore resulted only in its retraction. The first description of synchronized polypide protrusion and retraction in colonies of marine bryozoans was published by George Johnston in 1838.

In P.N. Wyse Jackson & M.E. Spencer Jones (eds), Annals of Bryozoology: aspects of the history of research on bryozoans (International Bryozoology Association, Dublin, 2002), pp. 185–199. 186 ANNALS OF BRYOZOOLOGY

Similarly to Dumortier, he also mentioned that ‘if, when many [polypides] are expanded [in a colony], one is…touched with a sharp instrument, it alone feels an injury and retires, without any others being conscious of the danger’.3 But in spite of the intensive studies on different taxa of these colonial using live specimens (Hassall,4 Dalyell,5 Gosse,6 Busk,7 Allman,8 Smitt,9 ,10 Hyatt,11 Nitsche,12 -15 Vigelius,16 Kraepelin,17 Pergens,18 Oka,19 Proucho,20 Calvet,21 Gerwerzhagen,22 Borg,23 etc.)24 there are only occasional remarks concerning group autozooidal behaviour in the literature published. For instance, Thomas Hincks25 and Fritz Müller26 mentioned ‘common and simultaneous movements’ of the autozooids in the ctenostome Mimosella gracilis Hincks.27, 28 ,29

3. Twentieth century studies

Folke Borg described removal of released eggs by their consecutive transference from lophophore to lophophore in a colony of the cheilostome pilosa (Linnaeus).30 Ernst Marcus made some observations on bryozoan behaviour during his experiments on several of both marine and fresh-water bryozoans, including the cheilostome E. pilosa, the ctenostome Farrella repens (Farre), and the phylactolaemates Cristatella mucedo Cuvier and Fredericella sultana (Blumenbach).31, 32 One of his main conclusions was that there is no colonial co-ordination in gymnolaemate Bryozoa, and that, as in the case of Johnston,33 no autozooid responded to a stimulus applied to any other.34 In contrast, the transmissions of stimuli from one member of a colony to another was demonstrated by Marcus for the phylactolaemates mentioned.35 Results of Marcus’s studies were regarded as being of the greatest importance by several authors36, 37, 38 in spite of the opinion of Georges Bronstein who claimed to have observed colonial responses in the ctenostome Bowerbankia sp.39 Also the data of Stanislaw Hiller, who described the interzooidal nervous connections in E. pilosa and E. crustulenta (Pallas) (both as Membranipora) and group polypide retractions after the stimulation of the frontal cystid wall,40 were considered as insufficient to cast doubt upon the conclusions of Marcus.41 Collective movements of entire zooids and whole zoarial branches resulting in a change of their orientation were investigated in detail by Lars Silén42 in ctenostomes of the genera Mimosella and Farrella and the cheilostome Kinetoskias correspondingly.43 However, Silén supported Marcus’s44 view, stating that mechanical stimulation of a zooid does not trigger any response from adjacent zooids.45, 46 Thus, the opinion about the absence of colonial co-ordination of zooidal activity survived for about 50 years in spite of the facts that there are momentary simultaneous polypide retractions after stimulation47-52 as well as movements of cheilostome bryozoan vibracula that can beat in unison.53-59 For instance, Silén believed that synchronous action of the vibracula in the cheilostome Caberea is a kind of metachronal chain reaction during which very long vibracular setae inevitably touch neighbouring ones that thereupon respond.60, 61, 62

Further investigations led researchers to suppose that the behaviour of Bryozoa is a very flexible and sensitive system of reactions that combines diverse individual and group COLONIAL BEHAVIOUR IN BRYOZOA 187 zooidal activities depending on the situation. At the present time, there are a lot of both morphological and behavioural evidences in favour of existence of the presumed colonial co-ordination in all main Recent bryozoan taxa. In addition to the anatomical data of earlier authors 63-71 many new facts that are indicative of nervous connections and transmission of nervous signals between zooids were obtained by Geneviève Lutaud,72- 80 who supported the hypothesis of interzooidal information spreading through a colony and leading to colonial responses.81

In the phylactolaemate Plumatella fungosa (Pallas) George Mackie recorded the phenomenon in which ‘the lophophores over wide regions become orientated by muscular action so that they point in the same direction’.82 He also mentioned co-ordinated withdrawal responses in Cristatella mucedo. Colonial behaviour and nervous responses were studied in some species of free-living cheilostome.83-87 Colonies under investigation showed a high degree of co-ordination of avicularian setae movement owing to which they were able to stop themselves being buried in sand, to return back to a normal position after being placed upside down, to travel across the aquarium preferably towards the light and to climb one over another.88 A high level of co-ordination was also recorded between autozooids, and between autozooids and avicularia, when feeding periods ending in simultaneous polypide retraction are alternated with simultaneous setal cleaning movement after which the colonial feeding is resumed. Co-ordinated avicularian activity in Recent lunulitiform bryozoans (Cupuladriidae) was also noted by Ernst and Eveline Marcus,89 Patricia Cook90 and Ronald Greeley.91 Judith Winston and Patricia Cook recorded synchronous movements of avicularian setae in different species of .92- 95

Collective activity of another type of bryozoan polymorphs was described by Lars Silén and Jean-Georges Harmelin who observed rocking and circular movements of the single tentacle of nanozooids in cyclostomes of the genera Plagioecia and Diplosolen.96 These movements were not synchronized but were simultaneous, and cleaned a colony surface after induced obstruction by silt. It was noted that the tentacles of nanozooids were the first to appear in the colony after strong disturbance, whereas autozooids expanded their lophophores much later. Similar ‘sentry’ behaviour performed solely by autozooids was also recorded in several cheilostomates.97

Some neurophysiological aspects of intra- and intercolonial co-ordination of behavioural responces were investigated in Membranipora membranacea (Linnaeus), Electra pilosa, Selenaria maculata (Busk) and Flustrellidra hispida (Fabricius).98-101 The long-term controversy (see above) was rejected at last. It was found in experiments that ‘mechanical [as well as electrical] stimulation of an extended lophophore…resulted solely in the retraction of that polypide’.102 In contrast, stimulation of the frontal membrane triggers ‘the immediate rapid withdrawal of all the extended lophophores within some distance of the zooid stimulated’.103, 104, 105 This is in good agreement with observations of Winston 188 ANNALS OF BRYOZOOLOGY who described group retractions during removal of large particles from a colony.106 Conduction of nerve pulses through the colony accompanied by quick consecutive retractions of polypides was proved both within the same colony107 -110 and within complexes of adjoining colonies.111 Moreover, such conduction was also shown in a representative of carnosan ctenostomes (F. hispida),112 although interzooidal nervous connections were not discovered by Lutaud who investigated Alcyonidium polyoum (Hassall).113 Michael Berry and Peter Hayward suggested that ‘the nervous activity responsible for co-ordinating locomotion would spread throughout the entire colony’ after their experiments with free-living S. maculata where strong illumination caused the colonies to start moving.114 Noticeably, in contrast with earlier observations115, 116, 117 John Thorpe found no obvious evidence for co-ordinated lophophore retractions in phylactolaemates.118 However, it has been found that co-ordinated autozooidal behaviour in Bryozoa is not limited to simultaneous protrusion-retraction excursions. Bryozoans are colonial organisms and, therefore, the effects of large numbers of individual lophophores may be readily seen. Collective feeding leads to several problems, e.g. how to prevent a repeated water filtration, and how to remove filtered water, sediment and wastes from a colony where an area with incurrent flow is many times larger than the excurrent area. This inequality potentially must result in an appearance of zones with high water pressure where normal zooidal functioning might be hampered. In such conditions it is conceivable that autozooids will somehow react in groups to alleviate the problems, and this might be considered as a consequence of colonial regulation. Colonial effects on feeding and behaviour of marine bryozoans have been intensively studied since the work of William Banta, Ken McKinney and Russell Zimmer who observed colonies of the cheilostome Membranipora sp. and noted that most of the colony was covered by extended polypides, but that there were numerous blank spaces (‘chimneys’).119 In these areas lophophores were not extended, while those around the edge of the chimney leaned away from its centre having the obliquely-truncated tentacle crowns with the longest tentacles bordering a chimney. The authors concluded that the incurrent water passed through the tentacles and down between the zooids exiting via the colony edge or a chimney. They also suggested that a formation of excurrent water outlets was connected with a colony size. In their opinion, in large colonies ‘lophophores…interfere with each other unless excurrent channels such as chimneys are present’.120 These researchers proposed that the monticules (maculae) known in some fossil stenolaemates might be such chimneys reflected in a skeleton, and this idea was supported and exploited by many researchers.121-132

Removal of filtered water from the colonies and co-ordinated autozooidal activity was further studied in detail by Patricia Cook and Jim Chimonides,133, 134 who examined 17 different species of the Recent marine bryozoans. For multiserial encrusting colonies they noted three patterns of excurrent flow: (1) active centripetal and centrifugal colony-wide flows, (2) “active” local excurrent flows from chimneys ringed by functioning autozooids with obliquely-truncated lophophores and (3) ‘passive’ chimneys or local exhalant flows COLONIAL BEHAVIOUR IN BRYOZOA 189 over areas devoid of actively feeding zooids. Their observations on M. membranacea led them to the opinion that both the position of chimneys in a colony and the position of obliquely-truncated lophophores in a chimney are astogenetically determined. In general, these researchers supposed that both astogenetic and ontogenetic (connected with a polypide recycling) changes are involved in production of various forms of filtered water outflows, and agreed with previous authors135, 136 that some reproductive processes might take part in chimney formation.137 Cook was the first to describe chimneys bordered by obliquely-truncated polypides that were tilted towards the chimney centre.138 Scott Lidgard, who conducted his experiments on Membranipora villosa Hincks, concluded that chimneys are an adaptation which allows colonies to minimise the recirculation of previously filtered water, making the colony more efficient.139 Matthew Dick proposed a hypothetical mechanism for chimney formation, suggesting that this process may involve both hydrodynamic and astogenetic control as well as their combination.140 He also showed the ways of transformation from obliquely-truncated lophophore to equitentacled one, and vice versa, in his study on Holoporella brunnea (Hincks) and M. serrilamella Osburn, and connected the reason for this transformation with lophophore position respectively to excurrent flow. Some problems of the spatial arrangement of feeding zooids and their interference in encrusing colonies were also investigated and discussed by John Thorpe and John Ryland141 and later by Daniel Grünbaum.142

Judith Winston investigated 79 species of Recent marine bryozoans and recognized six patterns of bryozoan colonial behaviour in relation to the morphology of polypides, their grouping, colony form and structure, and water currents produced.143, 144, 145 She distinguished species where colonies were characterized by (1) predominantly individualized polypide behaviour,146 (2) separated polypides whose orientation is controlled by the colony skeleton, (3) polypides forming temporary clusters, (4) polypides forming fixed clusters unreflected in the colony skeleton, (5) polypides forming fixed clusters enchanced by irregular skeletal patterning, (6) polypides forming fixed clusters enhanced by regular patterning of the colony skeleton. She also observed several earlier unknown manifestations of group autozooidal behaviour, and supported the hypothesis of Banta, McKinney and Zimmer147 recording an excurrent flow of filtered water above raised areas (knobs or monticules) in the skeleton of some cheilostomes.148, 149 This and subsequent work was reviewed by Frank McKinney150, 151, 152 who classified the feeding of 91 species of Bryozoa into four main categories. The first category includes those bryozoans that behave essentially as individuals when they feed. This often occurs when lophophores are sufficiently separated and do not act together with neighbours. Typically such lophophores are supported on long introverts (or elevated by tubular and erect distal ends of the cystids), radially symmetrical and equitentacled. The second category includes species where lophophores form temporary feeding clusters. In such cases only a fraction of the colony feeds at any time and clusters of lophophores form around an initially emerging lophophore. Alternatively, in the third category, lophophores are in fixed groups across a continuous colony surface, and in such colonies there is usually a high degree of 190 ANNALS OF BRYOZOOLOGY integrated behaviour. Invariably in such designs there are areas of outflow from the colony and in this category of Bryozoa there are often asymmetric lophophores found in these regions. The last category in which bryozoan colonies may be considered is that of skeletally separated lophophores, where a branching structure facilitates unidirectional flow towards the colony and between the branches. The lophophores may cover the area between the branches and lean over the space. There may also be a high degree of asymmetry in these lophophores and all of them typically have short introverts.

In her book, published in 1985, Patricia Cook mentioned the colonial behaviour in several cheilostomates. She was the first to describe the ‘colony-wide episodes of tentacle ‘reversal’’, when ‘the tentacle crowns were widely extended and the tips directed towards the colony surface’.153 Cook suggested that this behaviour pattern might be a colonial rejection, ‘correlated with reversal of ciliary movement, and may be associated with cleaning of detritus,154 sperm release or other, at present unknown functions’.155

Natalia Shunatova and Andrew Ostrovsky recorded group autozooidal reactions and colonial behaviour in 13 species and subspecies of marine bryozoans.156 Several collective reactions (synchronized scanning behaviour, repeated particle transference by circular water currents, feeding and cleaning of the colony surface by ‘chains’ of inclined lophophores) were described for the first time. In large colonies of Tegella armifera (Hincks) a new type of chimney was discovered. Chimneys are formed by temporary retraction of 10-12 neighbouring polypides, and the blank space is surrounded by equitentacled lophophores standing vertically. Chimneys associated with elevated areas on the colony surface (monticules) were found in Porella smitti (Kluge) and Schizomavella lineata (Nordgaard). But, in contrast to all previously published speculations and observations, the monticules were often places of incurrent rather than excurrent flow, and water outlets were formed in depressions between monticules. In S. lineata, monticules change their function from incurrent to excurrent after polypide degeneration. Shunatova and Ostrovsky suggested that elevated areas formed by frontal budding can probably change their function at least four times: (1) they can probably work as excurrent zones during the initial stages of formation when young monticules consist of only incipient zooids with non-functional polypides, (2) later they start to function as incurrent zones, (3) after polypide degeneration, they become excurrent zones, and (4) after polypide regeneration they function as incurrent zones again. The depressions between monticules would probably follow exactly the opposite succession. Thus, the hypothesis of Robert Anstey,157 who speculated that in some Palaeozoic stenolaemates the hydrodynamical regime around the monticules could change, was made more plausible.

Colony-wide water currents in relation to ambient flow, colony growth form and polypide morphology, distribution and behaviour were also intensively studied by Frank McKinney with co-authors in some Recent marine Bryozoa.158-163 The results fit well with previously proposed theoretical speculations concerning the interrelationship of the COLONIAL BEHAVIOUR IN BRYOZOA 191 ambient and cilia-generated water currents and growth forms in different fossil bryozoans.164-170 It was accepted that feeding was a ‘major sculptor of bryozoan form’.171, 172 Colony-wide water currents have been also considered to be very important in intra and interspecific competition.173, 174, 175

Beth Okamura and Julian Partridge supported Dick´s hypothesis176 of pressure build- up under the lophophore sheet in experiments with Membranipora membranacea. They showed “a trend towards [lophophore] miniaturization with increased flow: the zooids were less elongate, the lophophores were smaller in diameter and had fewer tentacles, and the distances between excurrent jets were shorter”.177

Colonial effects on feeding of some phylactolaemates have been studied by George Mackie,178 John Bishop and Leonard Bahr,179 Beth Okamura and Lita Doolan180 and Irina Antipenko.181, 182

4. Conclusions

In spite of many investigations, the only attempt to quantitatively estimate the degree of integration in bryozoan colonies was made by Frank McKinney.183 He used the extent of the colonial feeding current interactions for this purpose. Judith Winston proposed that the data on group behaviour of autozooids could be used for such estimation, and worked up a “matrix” where “levels of morphological and behavioural integration (with respect to feeding and current producing activities)” are considered.184, 185 Thus, previous research showed that bryozoans are a convenient model for investigations of different aspects of integrative processes. The data accumulated at the moment can be considered as a strong background for future research, and further observations on bryozoan behaviour as well as mathematical formalization should help to make progress in this direction.

5. Acknowledgements

We are greatly indebted to Professor Dr Claus Nielsen and Dr Mary E. Petersen, Zoological Museum, University of Copenhagen, and Mary Spencer Jones, The Natural History Museum, London, for kind help with literature. Our thanks to Drs William G. Sanderson, Michael A. Best and John P. Thorpe, Department of Environmental and Evolutionary Biology, University of Liverpool, Port Erin Marine Laboratory, for unpublished review on bryozoan feeding. We are grateful to Dr Ken McKinney, Appalachian State University and Dr Paul D. Taylor, The Natural History Museum, for reading and criticising earlier drafts of the manuscript, useful comments and much encouragement. Andrew N. Ostrovsky thanks the Danish Ministry of Education for a post- doctoral stipend which made work in the University of Copenhagen Library possible. The Otto Kinne Foundation is acknowledged for financial support. 192 ANNALS OF BRYOZOOLOGY

Notes

1H. Baker, Employment for the microscope (London, 1753), xiv, 442. 2B.-C. Dumortier, ‘Recherches sur l’anatomie et la physiologie des polypiers composés d’eau douce’, Bulletins de l’Académie Royale des Sciences, Bruxelles, 2 (1835), 421-454 (422). 3G. Johnston, ‘A history of the British zoophytes’ (Edinburgh, London, Dublin, 1838), 341 (36). 4 See: A.H. Hassall, ‘Supplement to a catalogue of Irish zoophytes’, The Annals and Magazine of Natural History, 7(44, 45) (1841), 276-287, 363-373 (Plate VI, figure 1). 5 J.G. Dalyell, Rare and remarkable animals of Scotland, represented from living subjects: with practical observations on their nature, 2 vols (Van Voorst, London, 1847-1848), vol 1, xii, 268, vol 2, iv, 322. 6P.H. Gosse, ‘Notes on some new or little-known marine animals’, The Annals and Magazine of Natural History, 2 Serie, 16 (1855), 27-36. 7G. Busk, ‘Zoophytology’, Quarterly Journal of Microscopical Science, 4 (1856), 308-312. 8G. Allman, A monograph of the fresh-water Polyzoa, including all the known species, both british and foreign (Ray Society, London, 1856), 120. 9F.A. Smitt, ‘Om Hafs-Bryozoernas utveckling och fettkroppar’, Öfversigt af Kongliga Vetenskapsakademien Förhandling, 1 (1865), 5-50. 10 F.A. Smitt, ‘Kritisk fürteckning öfver Skandinaviens Hafs-Bryozoer’, Öfversigt af Kongliga Vetenskapsakademien Förhandling, 2 (1865), 115-533. 11 A. Hyatt, ‘Observations on Polyzoa. Suborder Phylactolaemata’, Proceedings of the Essex Institute, vols 4 and 5 (Salem, 1866-1868), iv, 103. 12 H. Nitsche, Beiträge zur Anatomie und Entwickelungsgeschichte der phylactolaemen Süsswasserbryozoen, insbesondere von Alcyonella fungosa Pall., Akademisch Dissertation (Grimm and Maass, Berlin, 1868), 57. 13 H. Nitsche, ‘Beiträge zur Kenntnis der Bryozoen. I. Beobachtung über die Entwickelungsgeschichte einiger cheilostomen Bryozoen’, Zeitschrift für wissenschaftliche Zoologie, 20(1) (1869), 1-13. 14 H. Nitsche, ‘Beiträge zur Kenntnis der Bryozoen. IV. Über die Morphologie der Bryozoen’, Zeitschrift für wissenschaftliche Zoologie, 21 (1871), 92-119. 15 H. Nitsche, ‘Beiträge zur Kenntnis der Bryozoen. V. Über die Knospung der Bryozoen’, Zeitschrift für wissenschaftliche Zoologie, 25(supplement) (1876) 121-180. 16 W.J. Vigelius, ‘Morphologische Untersuchungen über Flustra membranaceo-truncata Smitt’, Biologisches Centrablatt, 23 (1884), 705-721. 17 K. Kraepelin, ‘Die Deutschen Süsswasser-Bryozoen. Anatomish-systematischer Teil’, Abhandlungen aus dem Gebiete der Naturwissenschaft herausgeben von dem Naturwissenschaftlicher Verein in Hamburg, 10 (1887), 1-168. 18 E. Pergens, ‘Untersuchungen an Seebryozoen’, Zoologischer Anzeiger 12 (1889), 504-510, 526-533. 19 A. Oka, ‘Observations on fresh-water Polyzoa. (Pectinatella gelatinosa, nov. sp.)’, Journal of the College of Science, Imperial University of Japan, Tokyo, 4 (1891), 89-150. 20 H. Proucho, ‘Contribution à l’histoire des Bryozoaires’, Archives de Zoologie expérimentale et générale, 10 (1892), 557-656. 21 L. Calvet, ‘Contribution à l’histoire naturelle des Bryozoaires Ectoproctes marins’, Travailes de l’Institut de Zoologie de l’Université de Montpellier, Nouvelle Série, 8 (1900), 1-488. 22 A. Gerwerzhagen, ‘Untersuchungen an Bryozoen’, Sitzungberichte der Heidelberger Akademie COLONIAL BEHAVIOUR IN BRYOZOA 193

der Wissenschaften, Matematische-naturwissenschaftliche Klasse B, 9 (1913), 1-16. 23 F. Borg, ‘On the structure of cyclostomatous Bryozoa’, Arkiv für Zoologie 15 (1923), 1-17. 24 For review see also: A.N. Ostrovsky, N.N. Shunatova, I.I. Antipenko, this volume. 25 T. Hincks, ‘Notes on British Zoophytes’, Annals and Magazine of Natural History, 2 Serie, 8 (1851), 353-362. 26 F. Müller, ‘On the common nervous system (Kolonialnervensystem) of the Bryozoa (Polyzoa), exemplified in Serialaria Coutinhii, n. sp.’, Quarterly Journal of Microscopical Science, New Series, 1 (1861), 300-305 (300). 27 See also H. Nitsche, ‘Beiträge zur Kenntnis der Bryozoen. III. Über die Anatomie und Entwickelungsgeschichte von Flustra membranacea’, Zeitschrift für wissenschaftliche Zoologie, 21 (1871), 37-91. 28 T. Hincks, ‘Contributions to history of Polyzoa.’, Quarterly Journal of Microscopical Science, (N. S.) 13 (1873), 13-37. 29 T. Hincks, A history of the British marine Polyzoa, 2 volumes (Van Voorst, London, 1880), 601. 30 F. Borg, ‘Studies on recent cyclostomatous Bryozoa’, Zoologiska Bidrag från Uppsala, 10 (1926), 181-150. 31 E. Marcus, ‘Beobachtungen und Versuche an lebenden Meersbryozoen’, Zoologische Jahrbücher Abteilung für Systematik, Ökologie und Geographie der Tiere, 52 (1926), 1-102. 32 E. Marcus, ‘Beobachtungen und Versuche an lebeden Sübwasserbryozoen’, Zoologische Jahrbücher Abteilung für Systematik, Ökologie und Geographie der Tiere, 52 (1926), 279-350. 33 Johnston, note 3. 34 Marcus, note 31. 35 Marcus, note 32. 36 L.H. Hyman, The invertebrates: smaller coelomate groups, 5 (McGraw-Hill Book Company, New York, Toronto, London, 1959), 275-515. 37 P. Brien, ‘Classe des Bryozoaires’, in Traité de Zoologie, edited by P.-P. Grasse, 5(2) (Masson et Sie, Paris, 1960), 1053-1335. 38 J.S. Ryland, Bryozoans (Hutchinson University Library, London, 1970), 175. 39 G. Bronstein, ‘Étude du système nerveux de quelques bryozoaires gymnolémides’, Travaux de la Station Biologique de Roscoff, 15 (1937), 155-174. 40 S. Hiller, ‘The so-called ‘colonial nervous system’ in Bryozoa’, Nature, 143 (3634) (1939), 1069-1070. 41 Summarized in J.P. Thorpe, ‘Bryozoa’, in Electrical conduction and behaviour in ‘simple’ invertebrates, edited by G.A.B. Shelton (Clarendon Press, Oxford, 1982), 393-439. 42 L. Silén, ‘On the motility of entire zooids in Bryozoa’, Acta Zoologica, 31 (1950), 349-386. 43 Reviewed by Hyman, note 36. 44 Marcus, note 31. 45 Silén, note 42. 46 L. Silén, ‘Polymorphism’, in Biology of Bryozoans, edited by R.M. Woollacott and R.L. Zimmer (Academic Press, London, New York, 1977), 183-231. 47 See Dumortier, note 2. 48 Johnston, note 3. 49 G. Johnston, ‘A history of the British zoophytes’, 2nd edition (Van Voorst, London, 1847), xiv, 488. 50 Bronstein, note 39. 51 Hiller, note 40. 194 ANNALS OF BRYOZOOLOGY

52 Summarized in T.H. Bullock and G.A. Horridge, ‘Bryozoa’, in Structure and function in the nervous systems of invertebrates, 1 (W. H. Freeman and Company, San Francisco, London, 1965), 632-647. 53 C.R. Darwin, Journal of researches into the geology and natural history of the various countries visited by H.M.S. Beagle under the command of Capt. Fitzroy, R.N., from 1832 to 1836 (Henry Colborn, London, 1839), 379. 54 C.R. Darwin, The origin of species by means of natural selection or the preservation of favoured races in the struggle for life (John Murray, London, 1872), 539. 55 G. Busk, ‘Remarks on the structure and function of the avicularian and vibracular organs of the Polyzoa; and on their value as diagnostic characters in the classification of those creatures’, Transactions of the Microscopical Society, New Series, 2 (1854), 26-34. 56 T. Hincks, ‘Note on the movements of the vibracula in Caberea Boryi, and on the supposed common nervous system in the Polyzoa’, Quarterly Journal of Microscopical Science, New Series, 18 (1878), 7-9. 57 Hincks, note 29. 58 A. Forbes, ‘Conditions affecting the response of the avicularia of Bugula’, Biological Bulletin, 65 (1933), 469-479. 59 Summarized in Hyman, note 36. 60 Silén, note 42. 61 Silén, note 46. 62 See also P.L. Cook, ‘Bryozoa from Ghana’, Zoologische Wetenschappen Musee Royal l’Afrique centrale Tervuren, Belgique, 238 (1985), 1-315. 63 A. Gerwerzhagen, ‘Beiträge zur Kenntnis der Bryozooen. I. Das Nervensystem von Cristatella mucedo Cuv.’, Zeitschrift für Wissenschaftliche Zoologie, 107 (1913), 309-45. 64 Marcus, note 31. 65 Marcus, note 32. 66 E. Marcus, ‘Über Lophopus crystallinus (Pall.)’, Zoologische Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere, 58 (1934), 501-606. 67 Bronstein, note 39. 68 Hiller, note 40. 69 C.I. Cori, ‘Ordnung der Tentaculata: Bryozoa’, in Handbuch der Zoologie III, 2(5) (Walter de Gruyter and Company, Berlin, 1941), 263-374, 375-503. 70 See also C.W.F. Krukenberg, Vergleichend-physiologische Studien, Experimentelle Untersuchungen von C.F.W. Krukenberg (Winter, Heidelberg, 1887), 517. 71 Brien, note 37. 72 G. Lutaud, ‘Le “plexus” parietal de Hiller et la coloration du système nerveux par le bleu de méthylène chez quelques Bryozoaires Chilostomes’, Zeitschrift für Zellforschung und mikroskopische Anatomie Abteilung, 99 (1969), 302-314. 73 G. Lutaud, ‘Le plexus parietal des Ctenostomes chez Bowerbankia gracilis Leydi (Vesicularines)’, Cahiers de Biologie Marine, 15 (1974), 403-408. 74 G. Lutaud, ‘L’innervation des parois de la loge chez Flustra papyracea (Ellis and Solander), (Bryozoaire Chilostome)’, Cahiers de Biologie Marine, 17 (1976), 337-346. 75 G. Lutaud, ‘The bryozoan nervous system’, in Biology of Bryozoans, edited by R.M. Woollacott and R.L. Zimmer (Academic Press, London, New York, 1977), 377-410. 76 G. Lutaud, ‘The probability of a plexus in the calcified wall of Crisidia cornuta (Linné)’, in Advances in Bryozoology, edited by G.P. Larwood and M.B. Abbot (Academic Press, London, COLONIAL BEHAVIOUR IN BRYOZOA 195

1979), 33-46. 77 G. Lutaud, ‘Etude ultrastructurale du ‘plexus colonial’ et recherche de connexions nerveuses interzoidiales chez le Bryozoaire Chilostome Electra pilosa (Linné)’, Cahiers de Biologie Marine, 20 (1979), 315-324. 78 Summarized in Thorpe, note 41. 79 R.S. Boardman, A.H. Cheetham, D.B. Blake, J. Utgaard, O.L. Karklins, P.L. Cook, P.A. Sandberg, G. Lutaud, and T.S. Wood, ‘Bryozoa’ (Part G, revised), in Treatise on Invertebrate Paleontology, edited by R.A. Robison, 1 (Geological Society of America, Boulder, Colorado and University of Kansas, Lawrence, 1983), 1-625. 80 H. Mukai, K. Terakado and C.G. Reed, ‘Bryozoa’, in Microscopic Anatomy of Invertebrates, edited by F.W. Harrison, 13 (Wiley-Liss, New York, 1997), 45-206. 81 Lutaud, note 75. 82 G.O. Mackie, ‘Siphonophores, bud colonies and superorganisms’, in The Lower Metazoa Comparative Biology and Phylogeny, edited by E.C. Dougherty (University of California Press, Berkeley, 1963), 329-336 (332). 83 P.L. Cook and P.J. Chimonides, ‘Observations on living colonies of Selenaria (Bryozoa, Cheilostomata). I’, Cahiers de Biologie Marine, 19 (1978), 147-158. 84 J.E. Winston, ‘Polypide morphology and feeding behaviour in marine ectoprocts’, Bulletin of Marine Science, 28(1) (1978), 1-31. 85 P.J. Chimonides and P.L. Cook, ‘Observations on living colonies of Selenaria (Bryozoa, Cheilostomata). II’, Cahiers de Biologie Marine, 22 (1981), 207-219. 86 M.S. Berry and P.J. Hayward, ‘Nervous and behavioural responses to light in colonies of the free-living bryozoan, Selenaria maculata (Busk)’, Experientia, 40 (1984), 108-110. 87 For discussion see also: P.L. Cook, ‘Some problems in interpretation of heteromorphy and colony integration in Bryozoa’, in Biology and Systematics of Colonial Organisms, edited by G.P. Larwood and B.R. Rosen, Systematics Association Special vol 11 (Academic Press, London, New York, 1979), 193-210. 88 Summarized in Thorpe, note 41. 89 E. Marcus and Ev. Marcus, ‘On some lunulitiform Bryozoa’, Boletim da Faculdade de Filosofia, Ciências e Letras, Universidade de São Paulo, Zoologia, 24 (1962), 281-312. 90 P.L. Cook, ‘Observations on live lunulitiform zoaria of Polyzoa’, Cahiers de Biologie Marine, 4 (1963), 407-413. 91 R. Greeley, ‘Natural orientation of lunulitiform bryozoans’, Bulletin of the Geological Society of America, 78 (1967), 1179-1182. 92 J.E. Winston, ‘Why bryozoans have avicularia – a review of the evidence’, Novitates of the American Museum of Natural History, 2789 (1984), 1-26. 93 J.E. Winston, ‘Victims of avicularia’, Marine Ecology, 7 (1986), 193-199. 94 J.E. Winston, ‘Avicularian behaviour – a progress report’, in Bryozoaires Actuels et Fossiles: Bryozoa Living and Fossil, edited by F.P. Bigey, Bulletin de la Société des Sciences Naturelles de l’Ouest de la France, Mémoire Hors Série, 1 (1991), 531-540. 95 Cook, note 62. 96 L. Silén and J.-G. Harmelin, ‘Observations on living Diastoporidae (Bryozoa Cyclostomata), with special regard to polymorphism’, Acta Zoologica, 55 (1974), 81-96. 97 N.N. Shunatova and A.N. Ostrovsky, ‘Group autozooidal behaviour and chimneys in marine bryozoans’, Marine Biology, 140 (2002), 503-518. 98 Reviewed in Thorpe, note 41. 196 ANNALS OF BRYOZOOLOGY

99 Mukai, Terakado and Reed, note 80. 100 For discussion see also: J.S. Ryland, ‘Physiology and ecology of marine bryozoans’, Advances in Marine Biology, 14 (1976), 285-443. 101 J.S. Ryland, ‘Structural and physiological aspects of coloniality in Bryozoa’, in Biology and Systematics of Colonial Organisms, edited by G.P. Larwood and B.R. Rosen, Systematics Association Special vol 11 (Academic Press, London, New York, 1979), 211-242. 102 J.P. Thorpe, G.A.B. Shelton and M.S. Laverack, ‘Electrophysiology and co-ordinated behavioural responses in the colonial bryozoan Membranipora membranacea (L.)’, Journal of Experimental Biology, 62 (1975), 389-404 (393). 103 J.P. Thorpe, ‘Behaviour and colonial activity in Membranipora membranacea (L.)’, in Bryozoa 1974, edited by S. Pouyet, Documents des Laboratoires de Géologie de la Faculte des Sciences de Lyon, 3 (1975), 115-121. 104 Thorpe, Shelton and Laverack, note 102, p. 393. 105 J.P. Thorpe, G.A.B. Shelton, and M.S. Laverack, ‘Colonial nervous control of lophophore retraction in cheilostome Bryozoa’, Science, 189 (1975), 80-1. 106 Winston, note 84. 107 Thorpe, note 103. 108 Thorpe, Shelton and Laverack, note 102. 109 Thorpe, Shelton and Laverack, note 105. 110 D.F. Shapiro, ‘Intercolony coordination of zooid behaviour and a new class of pore plates in a marine bryozoans’, Biological Bulletin, 182 (1992), 221-30. 111 Shapiro, note 110. 112 Thorpe, note 41. 113 G. Lutaud, ‘The innervation of the external wall in the carnosan ctenostome Alcyonidium polyoum (Hassall)’, in Recent and Fossil Bryozoa, edited by G.P. Larwood and C. Nielsen (Olsen and Olsen, Fredensborg, 1981), 144-150. 114 Berry and Hayward, note 86, p. 109. 115 Dumortier, note 2. 116 Marcus, note 32. 117 Mackie, note 82. 118 Thorpe, note 41. 119 W.C. Banta, F.K. McKinney and R.L. Zimmer, ‘Bryozoan monticules: excurrent water outlets?’, Science, 185 (1974), 783-784. 120 Banta, McKinney and Zimmer, note 119, p. 783. 121 P.D. Taylor, ‘Monticules in a Jurassic cyclostomatous bryozoan’, Geological Magazine, 112 (1975), 601-6. 122 P.D. Taylor, ‘The inference of extrazooidal feeding currents in fossil bryozoan colonies’, Lethaia, 12 (1979), 47-56. 123 P.D. Taylor, ‘Functional significance of contrasting colony form in two Mesozoic encrusting bryozoans’, Palaeogeography Palaeoclimatology Palaeoecology, 26 (1979), 151-158. 124 F.K. McKinney, ‘Functional interpretation of lyre-shaped Bryozoa’, Paleobiology, 3 (1977), 90-97. 125 F.K. McKinney, ‘Evolution of erect marine bryozoan faunas: repeated success of unilaminate species’, American Naturalist 128 (1986), 795-809. 126 F.K. McKinney, ‘Historical record of erect bryozoan growth forms’, Proceedings of the Royal Society, London, 228 (1986), 133-148. COLONIAL BEHAVIOUR IN BRYOZOA 197

127 R.L. Anstey, ‘Zooid orientation structures and water flow patterns in Paleozoic bryozoan colonies’, Lethaia, 14 (1981), 287-302. 128 R.L. Anstey, ‘Colony patterning and functional morphology of water flow in Paleozoic stenolaemate bryozoans’, in Bryozoa: Present and Past, edited by J.R.P. Ross (Western Washington University, Bellingham, WA, 1987), 1-8. 129 R.L. Anstey, ‘Astogeny and phylogeny: evolutionary heterochrony in Paleozoic bryozoans’, Paleobiology, 13 (1987), 20-43. 130 R.L. Anstey, J.F. Pachut, and D.R. Prezbindowski, ‘Morphogenetic gradients in Paleozoic bryozoan colonies’, Paleobiology, 2 (1976), 131-146. 131 M.E. Patzkowsky, ‘Inferred water flow patterns in the fossil Fistulipora M‘Coy (Cystoporata, Bryozoa)’, in Bryozoa: Present and Past, edited by J.R.P. Ross (Western Washington University, Bellingham, WA, 1987), 213-219. 132 F.K. McKinney and J.B.C. Jackson, Bryozoan evolution (University of Chicago Press, Chicago, London, 1989), 238. 133 P.L. Cook, ‘Colony-wide water currents in living Bryozoa’, Cahiers de Biologie Marine, 18 (1977), 31-47. 134 P. L. Cook and P.J. Chimonides, ‘Further observations on water current patterns in living Bryozoa’, Cahiers de Biologie Marine, 21 (1980), 393-402. 135 Banta, McKinney and Zimmer, note 119. 136 Taylor, note 121. 137 For review and discussion see Cook, note 87. 138 Cook, note 133. 139 S. Lidgard, ‘Water flow, feeding and colony form in an encrusting cheilostome’, in Recent and Fossil Bryozoa, edited by G.P. Larwood and C. Nielsen (Olsen and Olsen, Fredensborg, 1981), 175-182. 140 M.H. Dick, ‘A proposed mechanism for chimney formation in encrusting bryozoan colonies’, in Bryozoa: Present and Past, edited by J.R.P. Ross (Western Washington University, Bellingham, WA, 1987), 73-80. 141 J.P. Thorpe and J.S. Ryland, ‘Some theoretical limitations on the arrangement of zooids in encrusting Bryozoa’, in Bryozoa: Present and Past, edited by J.R.P. Ross (Western Washington University, Bellingham, WA, 1987), 276-283. 142 D. Grünbaum, ‘A model of feeding currents in encrusting bryozoans shows interference between zooids within a colony’, Journal of Theoretical Biology 174 (1995), 409-425. 143 Winston, note 84. 144 J.E. Winston, ‘Current-related morphology and behaviour in some Pacific coast bryozoans’, in Advances in Bryozoology, edited by G.P. Larwood and M.B. Abbott, Systematics Association Special vol 13 (Academic Press, London, New York, 1979), 247-268. 145 J.E. Winston, ‘Feeding behaviour of modern bryozoans’, in Studies in Geology 5: Lophophorates. Notes for a Short Course, edited by T.W. Broadhead (University of Tennessee, 1981), 1-21. 146 See also Cook, note 62. 147 Banta, McKinney and Zimmer, note 119. 148 Winston, note 84. 149 Winston, note 144. 150 F.K. McKinney, ‘Feeding and associated colonial morphology in marine bryozoans’, Reviews in Aquatical Science, 2 (1990), 255-280. 198 ANNALS OF BRYOZOOLOGY

151 F.K. McKinney, ‘Feeding currents of gymnolaemate bryozoans: better organization with higher colonial integration’, Bulletin of Marine Science, 34 (1984), 315-319. 152 See also P.D. Taylor, ‘Bryozoans’, in Functional Morphology of the Invertebrate Skeleton, edited by E. Savazzi (John Wiley and Sons Ltd, 1999), 623-46. 153 Cook, note 62, p. 29. 154 See description of the similar individual reaction in: N.N. Shunatova and A.N. Ostrovsky, ‘Individual autozooidal behaviour and feeding in marine bryozoans’, Sarsia, 86 (2001), 113-142. 155 Cook, note 62, p. 29. 156 Shunatova and Ostrovsky, note 97. 157 Anstey, note 127. 158 F.K. McKinney, M.R.A. Listokin and C.D. Phifer, ‘Flow and polypide distribution in the cheilostome Bugula and their inference in Archimedes’, Lethaia, 19 (1986), 81-93. 159 F.K. McKinney, M.J. McKinney and M.R.A. Listokin, ‘Erect bryozoans are more than baffling: enchanced sedimentation rate by a living unilaminate branched bryozoan and possible implications for fenestrate bryozoan mudmounds’, Palaios, 2 (1987), 41-47. 160 F.K. McKinney, ‘Planar branch systems in colonial suspension feeders’, Paleobiology, 7 (1981), 344-354. 161 F.K. McKinney, ‘Two patterns of colonial water flow in an erect bilaminate bryozoan, the cheilostome Schizotheca serratimargo (Hincks, 1886)’, Cahiers de Biologie Marine 30 (1989), 35-48. 162 F.K. McKinney, ‘Colonial feeding currents of Exidmonea atlantica (Cyclostomata)’, in Bryozoaires Actuels et Fossiles: Bryozoa Living and Fossil, edited by F.P. Bigey, Bulletin de la Société des Sciences Naturelles de l’Ouest de la France, Mémoire Hors Série, 1 (1991), 263-270. 163 F.K. McKinney, ‘How phylogeny limits function - the example of Exidmonea’, National Geographic Research and Exploration, 7 (1991), 432-441. 164 McKinney, note 124. 165 McKinney, note 160. 166 McKinney, note 125. 167 McKinney, note 126. 168 McKinney, Listokin and Phifer, note 158. 169 See also R. Cowen, J. Rider, ‘Functional analysis of fenestellid bryozoan colonies’, Lethaia, 5 (1972), 145-164. 170 J.F. Stratton and A.S. Horowitz, ‘Studies of the flow of water through models of Polypora’, in Bryozoa 1974, edited by S. Pouyet, Documents des Laboratoires de Géologie de la Faculte des Sciences de Lyon, 3 (1975), 425-438. 171 McKinney, note 150. 172 McKinney and Jackson, note 132, p. 238 (Chapter 6). 173 L.W. Buss, ‘Bryozoan overgrowth interactions – the interdependence of competition for space and food’, Nature, 281 (5731), (1980), 475-477. 174 J.E. Winston and J.B.C. Jackson, ‘Life histories of cryptic reef bryozoans’, in Recent and Fossil Bryozoa, edited by G.P. Larwood and C. Nielsen (Olsen and Olsen, Fredensborg, 1981), 317-318. 175 J.B.C. Jackson and J.E. Winston, ‘Ecology of criptic coral reef communities I. Distribution and abundance of major groups of encrusting organisms’, Journal of Experimental Marine COLONIAL BEHAVIOUR IN BRYOZOA 199

Biology and Ecology, 57 (1982), 135-147. 176 Dick, note 140. 177 B. Okamura and J.C. Partridge, ‘Suspension feeding adaptations to extreme flow environments in a marine bryozoan’, Biological Bulletin 196 (1999), 205-215 (205). 178 Mackie, note 82. 179 J.W. Bishop and L.M. Bahr, ‘Effects of colony size on feeding by Lophopodella carteri (Hyatt)’, in Colonies: Development and Function through Time, edited by R.S. Boardman, A.H. Cheetham and W.A. Oliver (Dowden, Hutchinson and Ross, Stroudsberg, PA, 1973), 433-437. 180 B. Okamura and L.A. Doolan, ‘Patterns of suspension feeding in the freshwater bryozoan Plumatella repens’, Biological Bulletin, 184 (1993), 52-56. 181 I.I. Antipenko, Feeding and behaviour of some fresh-water bryozoan species (Bryozoa, Phylactolaemata), Unpublished MSc Thesis, (St. Petersburg State University, 1998), 112 (in Russian). 182 For further discussion see Shunatova and Ostrovsky, note 97. 183 McKinney, note 151. 184 Winston, note 84, p. 30. 185 Winston, note 144. 200 ANNALS OF BRYOZOOLOGY